Research Article |
Corresponding author: Elizabeth A. Bowman ( eabowman@utexas.edu ) Academic editor: Harald Auge
© 2023 Elizabeth A. Bowman, Robert M. Plowes, Lawrence E. Gilbert.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Bowman EA, Plowes RM, Gilbert LE (2023) Evidence of plant-soil feedback in South Texas grasslands associated with invasive Guinea grass. NeoBiota 81: 33-51. https://doi.org/10.3897/neobiota.81.86672
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Plant-soil feedback (PSF) processes play an integral role in structuring plant communities. In native grasslands, PSF has a largely negative or stabilizing effect on plant growth contributing to species coexistence and succession, but perturbations to a system can alter PSF, leading to long-term changes. Through changes to soil abiotic and biotic properties, invasion by non-native plants has a strong impact on belowground processes with broad shifts in historical PSFs. Guinea grass, Megathyrsus maximus, an emerging invasive in South Texas, can efficiently exclude native plants in part due to its fast growth rate and high biomass accumulation, but its impacts on belowground processes are unknown. Here, we provide a first look at PSF processes in South Texas savannas currently undergoing invasion by Guinea grass. In this pilot study, we addressed the question of how the presence of the invasive M. maximus may alter PSF compared to uninvaded grasslands. Under greenhouse conditions, we assessed germination and growth of Guinea grass and the seed bank in soil collected from grasslands invaded and uninvaded by Guinea grass. We found that Guinea grass grown in soil from invaded grasslands grew taller and accumulated higher biomass than in soil from uninvaded grasslands. Plants grown from the seed bank were more species rich and abundant in soil from uninvaded grasslands but had higher biomass in soil from invaded grasslands. In South Texas savannas, we found evidence to support shifts in the direction of PSF processes in the presence of Guinea grass with positive feedback processes appearing to reinforce invasion and negative feedback processes possibly contributing to species coexistence in uninvaded grasslands. Future work is needed to determine the mechanisms behind the observed shifts in PSF and further explore the role PSF has in Guinea grass invasion.
bulk soil, grassland, Guinea grass, invasive species, Megathyrsus maximus, Panicum maximum, plant-soil feedback, South Texas
Invasive species are an increasingly widespread concern due to their negative impacts on ecosystems and difficulty in controlling their spread (
By modifying the abiotic and biotic qualities of their soil environment, plants can influence the establishment and growth of subsequent generations of plants within that same soil environment in a process termed plant-soil feedback (PSF) (
In South Texas, Guinea grass, Megathyrsus maximus (Jacq.) B.L. Simon and Jacobs, is emerging as a problematic invasive (
Our goal was to assess the study system in South Texas for evidence of PSF in grasslands invaded and uninvaded by Guinea grass specifically addressing the question: how does the presence of invasive Guinea grass alter PSF compared to uninvaded grasslands? Overall, aboveground contributions to the high competitive ability of Guinea grass are well documented (
To test our hypotheses, we conducted a greenhouse experiment that used soil collected in August 2020 from grasslands invaded by Guinea grass, Megathyrsus maximus, and uninvaded grasslands in Kleberg County, Texas (27.433, -97.67). Here in its unmanipulated state, grasses form the matrix of a savanna punctuated by clumps or mottes of diverse shrubs and low trees dominated by mesquite (Prosopis glandulosa). The area receives on average 73.6 cm of rain per year (Weather Service). Sampled grasslands were located between 4 to 8 km apart, spanning an area of approximately 5.5 km2. Soil from the three sites sampled in this study was composed predominantly of sand (mean 92% ± 1.8%) with minor amounts of silt and clay (mean 5.7% ± 0.8% and 2.3% ± 1.5%, respectively). Two of the sample sites were in grasslands that had remained intact at least since the 1980’s, while the third site had been mechanically treated in 2000 to partially remove encroaching mesquite (Suppl. material
Within each of three sites, we sampled soil from plots invaded by Guinea grass and uninvaded plots (i.e., predominantly native with no Guinea grass present) (n = 6) that were located within 10 m of each other to minimize the confounding effects of distance on soil microbial communities or soil traits (Suppl. material
For our experiment, we chose to use bulk soil due to concerns that autoclaving impacts soil nutrient availability and composition/abundance of microbial communities. To confirm the effect autoclaving has on soil nutrient availability, we conducted a small assessment on soil nutrients in the bulk soil pre-autoclaving and after two autoclave times (30 minutes and 60 minutes). We found that autoclaving increased levels of phosphorus, sulfur, sodium, and electrical conductivity with autoclave time (ANOVA results in Suppl. material
Since we were unable to refrigerate the bulk soil due to its large quantity, we added inoculum that was kept at 4 °C to counter any changes in the microbial community in the bulk soil. For this, we created two sets of inoculums: a pooled inoculum referred to hereafter as a mixed soil sample (MSS) and an unpooled inoculum referred to as an individual soil sample (ISS). To create the MSS inoculum, we pooled inoculum at a 1:1 ratio based on soil origin (invaded or uninvaded grasslands) for each of the three sites to create a common inoculum that was applied to replicates (n = 6 inoculum pools used for MSS treatments). For ISS inoculum, we used distinct (i.e., unpooled) soil cores for each replicate.
For the experiment, treatments included soil origin (invaded grassland, uninvaded grassland) and soil handling method (ISS, MSS). Each cross was replicated five times with soil from three separate sites (20 samples per site, 60 samples total). We filled black plastic pots (2.4 L) with the same amount of unautoclaved bulk soil (2640 g) and then added the additional soil inoculum (3% mass: mass; 79.2 g) to each pot (
In each pot, we sowed approximately 0.015 g of Guinea grass seed collected from the same area and time in South Texas. Although we were unable to quantify the seed bank, we used the same amount of soil in each pot to normalize the seed bank. During the sieving process, we homogenized the bulk soil based on site and soil origin as described above, then placed the same amount of bulk soil and inoculum as stated above into each pot. We visually assessed the sieved litter for seeds to ascertain whether larger seeds were removed during soil sieving (i.e. size sorting of seeds), but noted only plant leaves and roots in the material were removed during sieving.
After three weeks, we counted the total number of Guinea grass seedlings and thinned them to a single seedling per pot. At this stage the seedlings were approximately 5 cm tall and could be identified as Guinea grass. After this point, any new Guinea grass that emerged was counted and then removed from the pot. We monitored growth of these seedlings over the course of the experiment (14 weeks), after which plants were carefully removed from pots to keep as much of the root intact as possible. We measured the plant height at the end of the experiment, then separated the aboveground tissue from roots at the root collar and placed both in a drying oven at 65 °C for 3–5 days in labeled paper bags. We measured the dry weight of both above- and below-ground tissue.
We monitored the total number of plant seedlings sprouting from the seed bank weekly. At the end of the experiment, we counted the number of plants present within each pot noting how many were monocots and dicots. We were unable to identify seedlings to species as the plants were juveniles and did not have flowering structures. Therefore, to quantify species richness, we used phenotypic differences to distinguish morphospecies within each pot (hereafter, referred to as species richness) (
All statistical analyses were conducted in R and code is available for reproducibility. All data and scripts used for analyses are available on GitHub (eabowman/Bowmanetal-STexasGuineaGrass-PlantSoilFeedback) or at https://doi.org/10.5281/zenodo.7487382. To assess the effect of soil origin (invaded or uninvaded grasslands) and soil handling method on Guinea grass growth and germination, we used a mixed effect model to analyze germination, height, root length, and dry biomass. We treated soil origin and soil handling method as fixed variables and site as a random variable. We considered Guinea grass germination rate as the total number of seedlings and did not normalize this number as we used the same mass of seeds (0.015 g) per pot. We evaluated all data for normality and homogeneity of variance prior to analysis. Germination, height, and biomass data were log-transformed prior to analysis. Three pots had no Guinea grass growth and were removed from analyses.
The effect of soil origin and soil handling method on germination and growth of the seedbank plant community was also assessed using mixed-effects models as above. Here we also treated germination as the total number of seedlings that germinated as the amount of bulk soil and inoculum used was the same across all treatments and replicates. As above, all data were assessed to see if they met the assumptions for parametric analysis. Germination counts and plant abundance were log-transformed prior to analysis, whereas species richness and biomass were transformed using the formula log (x + 1).
To assess for differences in soil characteristics as a function of invasion, we used a t-test and included only data from unautoclaved soil (n = 6 samples; 3 from invaded sites and 3 uninvaded sites). Electrical conductivity, phosphorus, and sulfur were log transformed prior to analysis.
We found a significant difference in Guinea grass growth between invaded and uninvaded sites (Fig.
Results of ANOVA mixed effect model to assess the effect of soil origin (invasion status) and soil handling method on Guinea grass germination and growth. Seedling count is the total seedling number of seedlings in the first three weeks.
Soil origin | Soil handling method | Interaction | ||||
---|---|---|---|---|---|---|
F1,51 | p | F1,51 | p | F1,51 | p | |
Seedling count | 0.71 | 0.4057 | 7.20 | 0.0098 | 2.44 | 0.1245 |
Height | 38.60 | < 0.0001 | 0.98 | 0.3278 | 0.00 | 0.9789 |
Root length | 14.55 | 0.0004 | 0.20 | 0.6601 | 0.39 | 0.5350 |
Biomass | 31.22 | < 0.0001 | 0.08 | 0.7852 | 0.03 | 0.8740 |
Guinea grass height (a), root length (b), and biomass (c) when grown in soil collected from i) grassland invaded by conspecifics and ii) uninvaded grasslands dominated by native species. Experimental pots (d) after 14 weeks with larger Guinea grass in soil from invaded grasslands (left). All data shown are non-transformed.
Plant abundance and species richness of plants from the seed bank were significantly higher in soil from uninvaded sites than invaded sites (Fig.
Results of ANOVA mixed effect model to assess the effect of soil origin (invasion status) and soil handling method on germination and growth of plants from the seedbank. Seedling count here is the total seedling number of seedlings in the first three weeks.
Soil origin | Soil handling method | Interaction | ||||
---|---|---|---|---|---|---|
F1,51 | p | F1,51 | p | F1,51 | p | |
Seedling count | 49.31 | < 0.0001 | 0.14 | 0.7116 | 4.52 | 0.0382 |
Plant abundance | 9.05 | 0.004 | 5.57 | 0.0219 | 3.09 | 0.0843 |
Total biomass | 51.65 | < 0.0001 | 4.26 | 0.0439 | 0.10 | 0.7539 |
Species richness | 4.52 | 0.0382 | 0.02 | 0.8877 | 0.08 | 0.7850 |
Seedling count (a), abundance (b), biomass (c), and species richness (d) of plants which emerged from the seedbank in soil from Guinea grass invaded and uninvaded grasslands. All data shown are non-transformed.
Plant abundance (a) and species richness (b) as a function of invasion and plant group. Monocot species richness and plant abundance were significantly higher in soil from uninvaded sites than invaded sites (species richness: Kruskal-Wallis = 13.4, p = 0.0002; plant abundance: Kruskal-Wallis = 18.1, p < 0.0001), whereas species richness and abundance of dicots showed no difference. All data shown here are non-transformed.
Guinea grass germination, seedbank plant abundance, and total biomass of the seedbank plant community showed significant differences between the two soil handling methods we tested. Soil handling method significantly influenced Guinea grass germination with MSS treatments having higher germination (mean 21 ± 15) than ISS treatments (mean 12 ± 11) (Suppl. material
We found no significant difference between soil nutrients in invaded and uninvaded sites, although some nutrients trended higher in invaded sites (Fig.
Soil characteristics as a function of invasion. None of the soil characteristics were significantly different based on soil origin although in general soil nutrients and characteristics were higher in soil from invaded sites. All data shown here are non-transformed. EC is electrical conductivity.
Our experiment presents initial and novel data on PSF processes in the mesquite savannas in South Texas, the impact of Guinea grass invasion on PSF in uninvaded grasslands, and the response of seedbanks to shifts in PSF. In line with our hypothesis, Guinea grass grew taller and accumulated more biomass when grown in soil from invaded grasslands than soil from uninvaded grasslands consistent with a positive PSF on conspecific plants post-invasion (Fig.
For a non-native to be a successful invader, it needs to be able to colonize, establish, and disseminate to new environments (
After germination, the successful establishment of non-native plants is reliant on their fast growth rate, competitive ability with native plants, and efficient resource usage (
Invasion has been shown to impact multiple functional guilds within soil microbial communities through several pathways (e.g. phytochemicals, litter inputs) thus altering community processes (reviewed in
Another possible contributing factor, not considered in this study, is allelopathy. Invasion of non-native plants may cause cascading effects on conspecific native species through allelopathy as examples of the novel weapons hypothesis (
In this initial study, we found evidence that the presence of Guinea grass alters PSF for con- and heterospecific plant species indicating that Guinea grass could reinforce through positive feedback processes. Negative PSFs in uninvaded grasslands were associated with higher species richness and abundance of the plants in the seedbank possibly contributing to species coexistence in native grasslands. We found evidence to suggest that positive PSFs observed in invaded grasslands could be reinforcing establishment of Guinea grass, although the mechanism needs to be explored further. Our results represent the first time PSF processes have been studied in South Texas savannas and show how Guinea grass, an emerging invasive within the southern United States, influences these processes reinforcing its own invasion.
We would like to thank L. Miksch for assistance with the experiment and comments on the manuscript; A. Leo and A. Rhodes for comments on manuscript; Neobiota editor H. Auge, reviewer J.R. De Long, and reviewer 2 for their thorough and constructive comments which greatly improved our manuscript; the Lee and Ramona Bass Foundation for funding; and B. DuPont, J. Rutledge and E. Grahmann for arranging access and providing insights into the Guinea grass invasion of the study area.
Soil sampling sites showing extent of Guinea grass patch (white boundary, I) and adjacent uninvaded grassland (N) with nearby mesquite tree mottes. Google Earth Imagery date 1/13/2014. Scale bar 70m.
Data type: figure
Initial germination of Guinea grass seed (a) and the seedbank (b) during week 1 was higher in soil from invaded sites than uninvaded sites. All data shown here are non-transformed.
Data type: figure
Effect of soil handling method on Guinea grass seedling count (a), native community plant abundance (b), and native community biomass (c). MSS: mixed soil sampling; ISS: individual soil sampling. All data shown are non-transformed.
Data type: figure
Results of one-way ANOVA examining the effect of autoclave time on soil characteristics. Electrical conductivity, phosphorus, and sulfur were log-transformed prior to analysis.
Data type: table
Results of t-test examining differences in soil characteristics between invaded and uninvaded sites. Electrical conductivity, phosphorus, and sulfur were log-transformed prior to analysis.
Data type: table